Does effective population size affect rates of molecular evolution : mitochondrial data for host/parasite species pairs in bees suggests not

Adaptive evolutionary theory argues that organisms with larger effective population size (Ne) should have higher rates of adaptive evolution and therefore greater capacity to win evolutionary arm races. However, in some certain cases, species with much smaller Ne may be able to survive besides their opponents for an extensive evolutionary time. Neutral theory predicts that accelerated rates of molecular evolution in organisms with exceedingly small Ne are due to the effects of genetic drift and fixation of slightly deleterious mutations. We test this prediction in two obligate social parasite species and their respective host species from the bee tribe Allodapini. The parasites (genus Inquilina) have been locked into tight coevolutionary arm races with their exclusive hosts (genus Exoneura) for ~15 million years, even though Inquilina exhibit Ne that are an order of magnitude smaller than their host. In this study, we compared rates of molecular evolution between host and parasite using nonsynonymous to synonymous substitution rate ratios (dN/dS) of eleven mitochondrial protein-coding genes sequenced from transcriptomes. Tests of selection on mitochondrial genes indicated no significant differences between host and parasite dN/dS, with evidence for purifying selection acting on all mitochondrial genes of host and parasite species. Several potential factors which could weaken the inverse relationship between Ne and rate of molecular evolution are discussed

Differential transcriptomic responses to heat stress in surface and subterranean diving beetles

Subterranean habitats are generally very stable environments, and as such evolutionary transitions of organisms from surface to subterranean lifestyles may cause considerable shifts in physiology, particularly with respect to thermal tolerance. In this study we compared responses to heat shock at the molecular level in a geographically widespread, surface-dwelling water beetle to a congeneric subterranean species restricted to a single aquifer (Dytiscidae: Hydroporinae). The obligate subterranean beetle Paroster macrosturtensis is known to have a lower thermal tolerance compared to surface lineages (CTmax 38°C cf. 42–46°C), but the genetic basis of this physiological difference has not been characterized. We experimentally manipulated the thermal environment of 24 individuals to demonstrate that both species can mount a heat shock response at high temperatures (35°C), as determined by comparative transcriptomics. However, genes involved in these responses differ between species and a far greater number were differentially expressed in the surface taxon, suggesting it can mount a more robust heat shock response; these data may underpin its higher thermal tolerance compared to subterranean relatives. In contrast, the subterranean species examined not only differentially expressed fewer genes in response to increasing temperatures, but also in the presence of the experimental setup employed here alone. Our results suggest P. macrosturtensis may be comparatively poorly equipped to respond to both thermally induced stress and environmental disturbances more broadly. The molecular findings presented here have conservation implications for P. macrosturtensis and contribute to a growing narrative concerning weakened thermal tolerances in obligate subterranean organisms at the molecular level

Development and evaluation of a custom bait design based on 469 single-copy protein-coding genes for exon capture of isopods (Philosciidae: Haloniscus)

Transcriptome-based exon capture approaches, along with next-generation sequencing, are allowing for the rapid and cost-effective production of extensive and informative phylogenomic datasets from non-model organisms for phylogenetics and population genetics research. These approaches generally employ a reference genome to infer the intron-exon structure of targeted loci and preferentially select longer exons. However, in the absence of an existing and well-annotated genome, we applied this exon capture method directly, without initially identifying intron-exon boundaries for bait design, to a group of highly diverse Haloniscus (Philosciidae), paraplatyarthrid and armadillid isopods, and examined the performance of our methods and bait design for phylogenetic inference. Here, we identified an isopod-specific set of single-copy protein-coding loci, and a custom bait design to capture targeted regions from 469 genes, and analysed the resulting sequence data with a mapping approach and newly-created post-processing scripts. We effectively recovered a large and informative dataset comprising both short (300 bp) exons, with high uniformity in sequencing depth. We were also able to successfully capture exon data from up to 16-year-old museum specimens along with more distantly related outgroup taxa, and efficiently pool multiple samples prior to capture. Our well-resolved phylogenies highlight the overall utility of this methodological approach and custom bait design, which offer enormous potential for application to future isopod, as well as broader crustacean, molecular studies

The evolution of communal behavior in bees and wasps : an alternative to eusociality

Beginning with Darwin (1859), a fundamental question for research on social insects has concerned the evolution of divergent phenotypes among already-sterile indiviuals (Linksvayer and Wade 2005). As reviewed in this volume, the caste-based (eusocial) societies of termites (Isoptera), and ants, wasps, and bees (Hymenoptera), have been extensively studied. A second question concerns the evolutionary origins of group life, for which appropriate foci are societies in which group members share a nest but work is not organized by caste differences (i.e. cooperative breeders and communal nesters)

Behavioural environments and niche construction : the evolution of dim-light foraging in bees

Most bees forage for floral resources during the day, but temporal patterns of foraging activity vary extensively, and foraging in dim-light environments has evolved repeatedly. Facultative dim-light foraging behaviour is known in five of nine families of bees, while obligate behaviour is known in four families and evolved independently at least 19 times. The light intensity under which bees forage varies by a factor of 108, and therefore the evolution of dim-light foraging represents the invasion of a new, extreme niche. The repeated evolution of dim-light foraging behaviour in bees allows tests of the hypothesis that behaviour acts as an evolutionary pacemaker. With the exception of one species of Apis, facultative dim-light foragers show no external structural traits that are thought to enable visually mediated flight behaviour in low-light environments. By contrast, most obligate dim-light foragers show a suite of convergent optical traits such as enlarged ocelli and compound eyes. In one intensively studied species (Megalopta genalis) these optical changes are associated with neurobiological changes to enhance photon capture. The available ecological evidence suggests that an escape from competition for pollen and nectar resources and avoidance of natural enemies are driving factors in the evolution of obligate dim-light foraging

Nest descriptions of Megalopta aegis (Vachal) and M. guimaraesi Santos & Silveira (Hymenoptera, Halictidae) from the Brazilian Cerrado

We present the first data on the nesting biology of Megalopta aegis and M. guimaraesi from southeastern Brazil. Nests were collected in the Area de Protecao Ambiental Agua Limpa, Bauru, Sao Paulo state. Our data suggest that nest architecture is conserved throughout all species of Megalopta. Two nests of M. guimaraesi consisted of a single female with brood. Of three M. aegis nests, two contained single females with brood and the third nest contained three adult females, with three times more brood than any single female nest. This observation suggests that social behavior in M. aegis is facultative, as known for other Megalopta species

Evidence for social nesting in neotropical ceratinine bees

Small carpenter bees (Ceratinini) are a key taxon to understanding the transition from subsocial to social behaviour, as all documented groups are long-lived and tend to their young periodically throughout development, though the behaviour of multiple lineages is little known. This study provides the first evidence for social nesting in three Neotropical species of Ceratina (Ceratinula) from Panama. Social nesting was associated with nest reuse, consistent with the hypothesis of kin associations, and the proportion of nests (per species) that displayed sociality was as follows: C. buscki 5 %; C. rectangulifera 0 %; C. tricolor 6 %; and C. zeteki 23 %. Sociality is always a low-frequency phenomenon in ceratinine bee populations, and generally represents a third or less of the population. The fact that the majority of colonies remain solitary indicates that solitary nesting is adaptive in the studied species

Nesting biology and social behavior of two Xenochlora bees (Hymenoptera: Halictidae: Augochlorini) from Peru

The augochlorine (Halictidae) bee genus Xenochlora is the diurnal sister group to the nocturnal Megalopta, both of which are stem-nesting halictid bees. Here we present notes on the nesting biology and social behavior in four nests of Xenochlora nigrofemorata and one nest of X. ianthina from Madre de Dios, Peru. All nests contained multiple females and dissections of X. nigrofemorata indicated within nest reproductive differentiation among females that is associated with body size. Size variation among females is conspicuous and a variety of morphometrics are examined to document it. A genal index is used to describe cephalic variation, and results are compared with seven other halictine bees. All morphometrics were investigated for measurement error. Nests of Xenochlora appear to be founded by single females and multifemale nests clearly exhibit parasocial behavior and we hypothesize that they temporally switch between semisocial, eusocial and possibly communal phases

Biology of a nocturnal bee, Megalopta atra (Hymenoptera: Halictidae; Augochlorini), from the Panamanian highlands

Bees of the genus Megalopta have gained attention as a result of their social nesting and nocturnal foraging. Seventeen nests of Meglaopta atra from the highlands of Chiriqui Province, Panama, were collected at the end of the dry season when brood rearing is expected to be at its peak. Most nests contained single females; within multifemale nests only one female possessed enlarged ovarioles, although some non‐reproductive individuals were inseminated. In two of these nests reproductive individuals were clearly larger in body size than nestmates, but body size variation and macrocephaly were equivalent to those found in other Neotropical augochlorines. There was no evidence of a non‐reproductive worker‐like caste and multifemale nests did not appear to be more productive than solitary nests, which may represent pre‐reproductive assemblages. Megalopta atra appears to be isolated by altitude from co‐geners common in Panama, this is discussed in comparison with temperate halictine bees, in which environmental clines separate solitary from social populations

Biology of a weakly social bee, Exoneura (Exoneurella) setosa (Hymenoptera: Apidae) and implications for social evolution in Australian allodapine bees

Australian allodapine bees provide excellent material for comparative approaches to understanding social evolution. The subgenus Exoneurella occupies a cladistically basal position in the Australian Exoneura group and comprises only four species. We describe sociality in one Exoneurella species, E. setosa, and combine this with other data to infer some patterns of social evolution in allodapines. E. setosa rears a first brood solitarily, although staggered brood production and the production of a second brood in some nests leads to a situation where older, recently emerged brood have the ability to help rear their younger siblings and this overlaps with opportunities to lay eggs. This is similar to the situation for two other phylogenetically distal species of Exoneurella, as well as for members of the genus Braunsapis, which is used as an outgroup for Exoneura. When combined with other studies, our results suggest that the opportunity for sib-rearing is a plesiomorphic trait for Australian allodapines and this has been largely lost in a distal subgenus, Exoneura sensu stricto. Instead, multifemale brood-rearing colonies in this latter group mostly comprise individuals of the same generation, and species exhibit large group size, univoltinism and kin cofounding. This suggests that evolution can favour semisociality and quasisociality, even when eusociality has already arisen